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Authors: André Kessler and Michael B. Mueller.
Plant Signaling & Behavior (2024)
Abstract: "Plant induced responses to environmental stressors are increasingly studied in a behavioral ecology context. This is particularly true for plant induced responses to herbivory that mediate direct and indirect defenses, and tolerance. These seemingly adaptive alterations of plant defense phenotypes in the context of other environmental conditions have led to the discussion of such responses as intelligent behavior. Here we consider the concept of plant intelligence and some of its predictions for chemical information transfer in plant interaction with other organisms. Within this framework, the flow, perception, integration, and storage of environmental information are considered tunable dials that allow plants to respond adaptively to attacking herbivores while integrating past experiences and environmental cues that are predictive of future conditions. The predictive value of environmental information and the costs of acting on false information are important drivers of the evolution of plant responses to herbivory. We identify integrative priming of defense responses as a mechanism that allows plants to mitigate potential costs associated with acting on false information. The priming mechanisms provide short- and long-term memory that facilitates the integration of environmental cues without imposing significant costs. Finally, we discuss the ecological and evolutionary prediction of the plant intelligence hypothesis."
Authors: Shaoqin Li, Li He, Yongping Yang, Yixin Zhang, Xiao Han, Yanru Hu and Yanjuan Jiang.
The Plant Cell (2024)
One-sentence summary: The NPR1–TGA3–ICE1 regulatory module represents an important step in salicylic acid signaling during cold-activated resistance of plants to pathogen attack.
Abstract: "Cold stress affects plant immune responses, and this process may involve the salicylic acid (SA) signaling pathway. However, the underlying mechanism by which low-temperature signals coordinate with SA signaling to regulate plant immunity remains unclear. Here, we found that low temperatures enhanced the disease resistance of Arabidopsis thaliana against Pseudomonas syringae pv. tomato DC3000. This process required INDUCER OF CBF EXPRESSION 1 (ICE1), the core transcription factor in cold-signal cascades. ICE1 physically interacted with NONEXPRESSER OF PATHOGENESIS-RELATED GENES 1 (NPR1), the master regulator of the SA signaling pathway. Enrichment of ICE1 on the PATHOGENESIS-RELATED GENE 1 (PR1) promoter and its ability to transcriptionally activate PR1 were enhanced by NPR1. Further analyses revealed that cold stress signals cooperate with SA signals to facilitate plant immunity against pathogen attack in an ICE1-dependent manner. Cold treatment promoted interactions of NPR1 and TGACG-BINDING FACTOR 3 (TGA3) with ICE1 and increased the ability of the ICE1–TGA3 complex to transcriptionally activate PR1. Together, our results characterize a critical role of ICE1 as an indispensable regulatory node linking low-temperature-activated and SA-regulated immunity. Understanding this crucial role of ICE1 in coordinating multiple signals associated with immunity broadens our understanding of plant–pathogen interactions."
Authors: Dacheng Wang, Lirong Wei, Jinbiao Ma, Kenichi Tsuda, Chunhao Jiang and Yiming Wang.
Cell Reports (2024)
Editor's view: The plant microbiome helps to shape the immune system to counter infection of pathogens. Wang et al. show that the root-associated Bacillus cereus NJ01 significantly enhances plant resistance. The EDS1-WRKY18 module is required for NJ01-enhanced disease resistance through activation of SA- and ABA-mediated immunity.
Highlights: • Rhizobacterium Bacillus cereus NJ01 enhances plant resistance against bacterial pathogens • EDS1 enhances WRKY18 DNA-binding activity for the NJ01-enhanced disease resistance • ICS1 and NCED3/5 are downstream of EDS1-WRKY18 for NJ01-enhanced disease resistance
Abstract: "Emerging evidence suggests a beneficial role of rhizobacteria in ameliorating plant disease resistance in an environment-friendly way. In this study, we characterize a rhizobacterium, Bacillus cereus NJ01, that enhances bacterial pathogen resistance in rice and Arabidopsis. Transcriptome analyses show that root inoculation of NJ01 induces the expression of salicylic acid (SA)- and abscisic acid (ABA)-related genes in Arabidopsis leaves. Genetic evidence showed that EDS1, PAD4, and WRKY18 are required for B. cereus NJ01-induced bacterial resistance. An EDS1-PAD4 complex interacts with WRKY18 and enhances its DNA binding activity. WRKY18 directly binds to the W box in the promoter region of the SA biosynthesis gene ICS1 and ABA biosynthesis genes NCED3 and NCED5 and contributes to the NJ01-induced bacterial resistance. Taken together, our findings indicate a role of the EDS1/PAD4-WRKY18 complex in rhizobacteria-induced disease resistance."
Authors: Cheng Zhang, Charles Tetteh, Sheng Luo, Pinyuan Jin, Xingqian Hao, Min Sun, Nan Fang, Yingjun Liu and Huajian Zhang.
Molecular Plant Pathology (2024)
Abstract: Pectin has been extensively studied in animal immunity, and exogenous pectin as a food additive can provide protection against inflammatory bowel disease. However, the utility of pectin to improve immunity in plants is still unstudied. Here, we found exogenous application of pectin triggered stomatal closure in Arabidopsis in a dose- and time-dependent manner. Additionally, pectin activated peroxidase and nicotinamide adenine dinucleotide phosphate (NADPH) oxidase to produce reactive oxygen species (ROS), which subsequently increased cytoplasmic Ca2+ concentration ([Ca2+]cyt) and was followed by nitric oxide (NO) production, leading to stomatal closure in an abscisic acid (ABA) and salicylic acid (SA) signalling-dependent mechanism. Furthermore, pectin enhanced the disease resistance to Pseudomonas syringae pv. tomato DC3000 (Pst DC3000) with mitogen-activated protein kinases (MPKs) MPK3/6 activated and upregulated expression of defence-responsive genes in Arabidopsis. These results suggested that exogenous pectin-induced stomatal closure was associated with ROS and NO production regulated by ABA and SA signalling, contributing to defence against Pst DC3000 in Arabidopsis.
Authors: Shai Morin, Peter W. Atkinson and Linda L. Walling.
Annual Review of Entomology (2024)
Abstract: "The rapid advances in available transcriptomic and genomic data and our understanding of the physiology and biochemistry of whitefly–plant interactions have allowed us to gain new and significant insights into the biology of whiteflies and their successful adaptation to host plants. In this review, we provide a comprehensive overview of the mechanisms that whiteflies have evolved to overcome the challenges of feeding on phloem sap. We also highlight the evolution and functions of gene families involved in host perception, evaluation, and manipulation; primary metabolism; and metabolite detoxification. We discuss the emerging themes in plant immunity to whiteflies, focusing on whitefly effectors and their sites of action in plant defense–signaling pathways. We conclude with a discussion of advances in the genetic manipulation of whiteflies and the potential that they hold for exploring the interactions between whiteflies and their host plants, as well as the development of novel strategies for the genetic control of whiteflies."
Authors: Yuli Du, Heng Zhang, Kunpeng Jia, Zongyan Chu, Shican Xu, Lam-Son Phan Tran, Jinggong Guo, Weiqiang Li and Kun Li.
Physiologia Plantarum (2024)
Abstract: "In terrestrial plants, stomata in the leaf epidermis formed by guard cells are the major pathways for gas exchange. However, opened stomata also provide a major channel for pathogen entry. At the pre-invasive stage, plants actively close stomata to prevent pathogen attack, which is termed stomatal immunity, and plant hormones are involved in this process. Here, we summarize recent advances in the role of abscisic acid (ABA) in promoting stomatal immunity to prevent pathogen entry. Additionally, salicylic acid shares common downstream elements with ABA to promote stomatal immunity, whereas reactive oxygen species and Ca2+ act as critical signals to cross-talk with ABA signalling to regulate stomatal movement, and they also enhance the effect of ABA in stomatal immunity. On the other hand, at the post-invasive stage, closed stomata create a water-soaked environment that allows pathogen multiplication, and ABA signalling is hijacked by pathogens to reduce stomatal aperture. Here, we propose a model of dual roles of ABA-mediated stomatal closure during plant-pathogen interaction and offer emerging consequences and questions for ABA-mediated stomatal immunity."
Authors: Steven H. Spoel and Xinnian Dong.
The Plant Cell (2024)
Abstract: "As the most widely used herbal medicine in human history and a major defense hormone in plants against a broad spectrum of pathogens and abiotic stresses, salicylic acid (SA) has attracted major research interest. With applications of modern technologies over the past 30 years, studies of the effects of SA on plant growth, development, and defense have revealed many new research frontiers, and continue to deliver surprises. In this review, we provide an update on recent advances in our understanding of SA metabolism, perception, and signal transduction mechanisms in plant immunity. An overarching theme emerges that SA executes its many functions through intricate regulation at multiple steps: SA biosynthesis is regulated both locally and systemically, while its perception occurs through multiple cellular targets, including metabolic enzymes, redox regulators, transcription cofactors, and most recently, an RNA-binding protein. Moreover, SA orchestrates a complex series of posttranslational modifications of downstream signaling components and promotes the formation of biomolecular condensates that function as cellular signaling hubs. SA also impacts wider cellular functions through crosstalk with other plant hormones. Looking into the future, we propose new areas for exploration on SA functions, which will undoubtedly uncover more surprises for many years to come."
Authors: Muhammad Arslan Mahmood, Muhammad Jawad Akbar Awan, Rubab Zahra Naqvi and Shahid Mansoor.
Trends in Plant Science (2024)
Abstract: "Stressed plants emit a variety of chemicals into the environment, leading to increased pest resistance in neighbouring plants but the genetic and molecular mechanisms of the emissions remain obscure. Recently, Gong et al. identified novel methyl salicylate (MeSA)-mediated airborne defence that confers resistance to neighbouring plants against aphids and viruses."
Authors: Mikayla Carty, Ruize Zhang, Ziyue Li, Daowen Wang and Zheng Qing Fu.
Molecular Plant (2023)
Excerpts: "Aphids are highly destructive pests that greatly hurt the agricultural industry. Transmitting over 40% of plant viruses, they are the most destructive pests that the agricultural industry faces (Gong et al., 2023). Aphids feed on plants, and in doing so, they consume sap from one plant and then move to another and inject their saliva into the new plant (Hooks and Fereres, 2006). This cycle causes diseases and viral pathogens to become rampant between plants as the aphids carry viral pathogens from one plant to another and so on. In response to this harmful process, plants release volatile organic compounds (VOCs) in order to elicit airborne defense (AD) mechanisms to counterstrike harmful aphids and aphid-transmitted viruses (Hooks and Fereres, 2006). A fascinating recent study published from Yule Liu’s lab revealed that methyl-salicylate (MeSA) serves as a VOC in the AD battle against aphids and viruses (Gong et al., 2023).
"Gong et al. discovered that phloem-feeding insects like aphids trigger a SA response in attacked plants, leading to an increase in SA levels (Gong et al., 2023). This SA increase activates the NAC2 transcription factor, which in turn binds to the SAMT1 promoter and induces the transcription of SAMT1, encoding the enzyme responsible for converting SA into MeSA (Figure 1A). This marks the start of the AD process. MeSA, as a predominant VOC induced by aphid attacks, will then reach the neighboring plants (Gong et al., 2023)."
"In response to this plant adaptation, some aphid-transmitted viruses have evolved mechanisms to suppress MeSA emission in aphid-attacked plants, impairing the induction of plant defenses against virus infection and aphid infestation in nearby plants and therefore effectively fighting against AD. This is accomplished through helicase-domain-containing proteins that interfere with NAC2. For example, CMV1a interacts with NAC2 and promotes NAC2 degradation through the 26S proteasome, disrupting the process that produces AD-inducing MeSA (Figure 1B) (Gong et al., 2023)."
Authors: Mengqian Lu, Yifan Zhao, Yingying Feng, Xiaoyan Tang, Wei Zhao, Keke Yu, Yuting Pan, Qiang Wang, Jilai Cui, Mengting Zhang, Jieyang Jin, Jingming Wang, Mingyue Zhao, Wilfried Schwab and Chuankui Song.
Advanced Science (2023)
Abstract: "The plant hormone salicylic acid (SA) plays critical roles in plant innate immunity. Several SA derivatives and associated modification are identified, whereas the range and modes of action of SA-related metabolites remain elusive. Here, the study discovered 2,4-dihydroxybenzoic acid (2,4-DHBA) and its glycosylated form as native SA derivatives in plants whose accumulation is largely induced by SA application and Ps. camelliae-sinensis (Pcs) infection. CsSH1, a 4/5-hydroxylase, catalyzes the hydroxylation of SA to 2,4-DHBA, and UDP-glucosyltransferase UGT95B17 catalyzes the formation of 2,4-DHBA glucoside. Down-regulation reduced the accumulation of 2,4-DHBA glucosides and enhanced the sensitivity of tea plants to Pcs. Conversely, overexpression of UGT95B17 increased plant disease resistance. The exogenous application of 2,4-DHBA and 2,5-DHBA, as well as the accumulation of DHBA and plant resistance comparison, indicate that 2,4-DHBA functions as a potentially bioactive molecule and is stored mainly as a glucose conjugate in tea plants, differs from the mechanism described in Arabidopsis. When 2,4-DHBA is applied exogenously, UGT95B17-silenced tea plants accumulated more 2,4-DHBA than SA and showed induced resistance to Pcs infection. These results indicate that 2,4-DHBA glucosylation positively regulates disease resistance and highlight the role of 2,4-DHBA as potentially bioactive molecule in the establishment of basal resistance in tea plants."
Authors: Siyu Song, Zayda Morales Moreira, Annika L. Briggs, Xue-Cheng Zhang, Andrew C. Diener and Cara H. Haney.
Nature Plants (2023)
One-sentence summary: To avoid autoimmunity against the microbiome, plants use PHYTOSULFOKINE RECEPTOR 1-mediated regulation of salicylic acid signalling to tune the plant growth–defence balance in response to microbiota.
Abstract: "Microbiota benefit their hosts by improving nutrient uptake and pathogen protection. How host immunity restricts microbiota while avoiding autoimmunity is poorly understood. Here we show that the Arabidopsis phytosulfokine receptor 1 (pskr1) mutant displays autoimmunity (plant stunting, defence-gene expression and reduced rhizosphere bacterial growth) in response to growth-promoting Pseudomonas fluorescens. Microbiome profiling and microbiota colonization showed that PSKR1-mediated reduction in bacterial growth and stunting is largely specific to Pseudomonas. Transcriptional profiling demonstrated that PSKR1 regulates the growth–defence trade-off during Pseudomonas colonization: PSKR1 upregulates plant photosynthesis and root growth but suppresses salicylic-acid-mediated defences. Genetic epistasis experiments showed that pskr1 stunting and restriction of bacterial growth are salicylic acid dependent. Finally, we showed that Pseudomonas, but not other bacteria, induces PSKR1 expression in roots, suggesting that Pseudomonas might manipulate plant signalling to promote its colonization. Our data demonstrate a genetic mechanism to coordinate beneficial functions of the microbiome while preventing autoimmunity.
Authors: Shiyi Xie, Hongbing Luo, Wei Huang, Weiwei Jin and Zhaobin Dong.
International Journal of Plant Biology (2024)
Abstract: "Maize (Zea mays) cultivation is strongly affected by both abiotic and biotic stress, leading to reduced growth and productivity. It has recently become clear that regulators of plant stress responses, including the phytohormones abscisic acid (ABA), ethylene (ET), and jasmonic acid (JA), together with reactive oxygen species (ROS), shape plant growth and development. Beyond their well-established functions in stress responses, these molecules play crucial roles in balancing growth and defense, which must be finely tuned to achieve high yields in crops while maintaining some level of defense. In this review, we provide an in-depth analysis of recent research on the developmental functions of stress regulators, focusing specifically on maize. By unraveling the contributions of these regulators to maize development, we present new avenues for enhancing maize cultivation and growth while highlighting the potential risks associated with manipulating stress regulators to enhance grain yields in the face of environmental challenges."
Authors: Lingya Yao, Zeyu Jiang, Yiping Wang, Yezhou Hu, Guodong Hao, Weili Zhong, Shiwei Wan and Xiu-Fang Xin.
The EMBO Journal (2023)
Synopsis: Many plant diseases are more severe when air humidity is high; however, the effect of air humidity on host plant biology remains obscure. This report shows that, in very humid conditions, key salicylic acid-mediated plant defenses are suppressed, making plants more vulnerable to infection. High humidity triggers a range of plant physiological responses. Investigating the effects of high humidity on individual plant immune pathways revealed a significant suppression of salicylic acid (SA) accumulation and signaling. Cellular ubiquitination pathways are suppressed in high humidity, including the ubiquitination and activity of the SA receptor NPR1.
Abstract: "The occurrence of plant disease is determined by interactions among host, pathogen, and environment. Air humidity shapes various aspects of plant physiology and high humidity has long been known to promote numerous phyllosphere diseases. However, the molecular basis of how high humidity interferes with plant immunity to favor disease has remained elusive. Here we show that high humidity is associated with an “immuno-compromised” status in Arabidopsis plants. Furthermore, accumulation and signaling of salicylic acid (SA), an important defense hormone, are significantly inhibited under high humidity. NPR1, an SA receptor and central transcriptional co-activator of SA-responsive genes, is less ubiquitinated and displays a lower promoter binding affinity under high humidity. The cellular ubiquitination machinery, particularly the Cullin 3-based E3 ubiquitin ligase mediating NPR1 protein ubiquitination, is downregulated under high humidity. Importantly, under low humidity the Cullin 3a/b mutant plants phenocopy the low SA gene expression and disease susceptibility that is normally observed under high humidity. Our study uncovers a mechanism by which high humidity dampens a major plant defense pathway and provides new insights into the long-observed air humidity influence on diseases."
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Author: Leiyun Yang
The Plant Cell (2024)
Excerpts: "Simultaneously, low temperature stimulates plant immunity by activating salicylic acid (SA)-mediated signaling (Wu et al. 2019). However, the mechanism by which plants integrate cold signals and immune signaling remain elusive. To investigate this question, Shaoqin Li and colleagues (Li et al. 2024) studied the potential involvement of ICE1 in cold-induced immunity in Arabidopsis."
"To elucidate how ICE1 regulates cold-induced immunity, the authors conducted a yeast-two-hybrid screen and identified NON-EXPRESSER OF PR GENES 1 (NPR1), a master transcriptional co-activator of PATHOGENESIS-RELATED GENE 1 (PR1) in SA-activated immunity, as an ICE1 interactor.....Additionally, the authors found that ICE1 directly binds to the PR1 promoter for gene activation. These results illustrate that ICE1 interacts with NPR1 and is required for SA-mediated immunity by directly promoting PR1 expression."
"These results support the conclusion that ICE1 and TGA3 work synergistically to promote PR1 transcription. This study not only shed light on a new role of ICE1 in SA-mediated immunity at low temperature, but also revealed NPR1-TGA3/ICE1 as an important nexus integrating SA signaling and cold signals in plant immunity (see Figure)."
Authors: Tingliang Xu, Xiaowen Zheng, Yi Yang, Shumin Yang, Xingwan Yi, Chao Yu, Le Luo, Jia Wang, Tangren Cheng, Qixiang Zhang and Huitang Pan.
Planta (2024)
Main conclusion: IAA cooperates with JA to inhibit SA and negatively regulates rose black spot disease resistance.
Abstract: "Black spot disease caused by the fungus Marssonina rosae is the most prevalent and severe ailment in rose cultivation, leading to the appearance of black spots on leaves and eventual leaf fall, significantly impacting the utilization of roses in gardens. Salicylic acid (SA) and jasmonic acid (JA) are pivotal hormones that collaborate with indole-3 acetic acid (IAA) in regulating plant defense responses; however, the detailed mechanisms underlying the induction of black spot disease resistance by IAA, JA, and SA remain unclear. In this study, transcript analysis was conducted on resistant (R13–54) and susceptible (R12–26) lines following M. rosae infection. In addition, the impact of exogenous interference with IAA on SA- and JA-mediated disease resistance was examined. The continuous accumulation of JA, in synergy with IAA, inhibited activation of the SA signaling pathway in the early infection stage, thereby negatively regulating the induction of effective resistance to black spot disease. IAA administration alleviated the inhibition of SA on JA to negatively regulate the resistance of susceptible strains by further enhancing the synthesis and accumulation of JA. However, IAA did not contribute to the negative regulation of black spot resistance when high levels of JA were inhibited. Virus-induced gene silencing of RcTIFY10A, an inhibitor of the JA signaling pathway, further suggested that IAA upregulation led to a decrease in disease resistance, a phenomenon not observed when the JA signal was inhibited. Collectively, these findings indicate that the IAA-mediated negative regulation of black spot disease resistance relies on activation of the JA signaling pathway."
Authors: Weiwei Cai, Yilin Tao, Xingge Cheng, Meiyun Wan, Jianghuang Gan, Sheng Yang, Thomas W. Okita, Shuilin He and Li Tian.
Plant Biotechnology Journal (2024)
Abstract: "To challenge the invasion of various pathogens, plants re-direct their resources from plant growth to an innate immune defence system. However, the underlying mechanism that coordinates the induction of the host immune response and the suppression of plant growth remains unclear. Here we demonstrate that an auxin response factor, CaARF9, has dual roles in enhancing the immune resistance to Ralstonia solanacearum infection and in retarding plant growth by repressing the expression of its target genes as exemplified by Casmc4, CaLBD37, CaAPK1b and CaRROP1. The expression of these target genes not only stimulates plant growth but also negatively impacts pepper resistance to R. solanacearum. Under normal conditions, the expression of Casmc4, CaLBD37, CaAPK1b and CaRROP1 is active when promoter-bound CaARF9 is complexed with CaIAA2. Under R. solanacearum infection, however, degradation of CaIAA2 is triggered by SA and JA-mediated signalling defence by the ubiquitin-proteasome system, which enables CaARF9 in the absence of CaIAA2 to repress the expression of Casmc4, CaLBD37, CaAPK1b and CaRROP1 and, in turn, impeding plant growth while facilitating plant defence to R. solanacearum infection. Our findings uncover an exquisite mechanism underlying the trade-off between plant growth and immunity mediated by the transcriptional repressor CaARF9 and its deactivation when complexed with CaIAA2."
Authors: Saumya Jaiswal, Durgesh Kumar Tripathi, Ravi Gupta, Jing He, Zhong-Hua Chen and Vijay Pratap Singh.
Journal of Integrative Plant Biology (2024)
Editor's view: After being infested by aphids, plants trigger a signaling pathway that involves methyl salicylate as an airborne signaling molecule. Thus, the regulation of communication for systemically acquired resistance produced via methyl salicylate is helpful in generating stress resistance among plants against aphid infestation.
Excerpts: "In this commentary, we discuss the signaling role of methyl-salicylate (MeSA) under attack by members of Aphidoidea in plants, which brings about systemically acquired resistance in the aphid-infested plant as well as neighboring plants by acting as a long-distance signaling molecule."
"On the other hand, elevated salicylic acid levels activate the Nicotiana benthamiana transcription factor 2 (NAC2), which gets attached to the promotor region of SAMT1 to activate its transcription process, resulting in conversion of salicylic acid into MeSA. MeSA is transferred via phloem to other plant parts or received by neighboring plants through some specific receptor-like salicylic acid binding protein 2 (SABP2), which also regulates the reconversion of MeSA into salicylic acid to generate specific response against pathogens and insects (Chen et al., 2020; Gong et al., 2023)."
"Although plants are proficient in responding to various environmental cues, MeSA is reported as the key player for interactions among neighboring plants as it is highly aquaphobic and volatile, more so than salicylic acid, along with generating the systemically adapted resilience in plants affected with aphids (Gong et al., 2023). Being a VOC, MeSA can be transferred aerially to neighboring plants in a species-specific manner to produce airborne defense (Gondor et al., 2022)."
Authors; Kohji Yamada and Akira Mine.
Science Advances (2024)
One-sentence summary: In plants, the types and amplitudes of defense outputs against bacterial and fungal pathogens depend on cellular sugars.
Abstract: "Pathogen recognition triggers energy-intensive defense systems. Although successful defense should depend on energy availability, how metabolic information is communicated to defense remains unclear. We show that sugar, especially glucose-6-phosphate (G6P), is critical in coordinating defense in Arabidopsis. Under sugar-sufficient conditions, phosphorylation levels of calcium-dependent protein kinase 5 (CPK5) are elevated by G6P-mediated suppression of protein phosphatases, enhancing defense responses before pathogen invasion. Subsequently, recognition of bacterial flagellin activates sugar transporters, leading to increased cellular G6P, which elicits CPK5-independent signaling promoting synthesis of the phytohormone salicylic acid (SA) for antibacterial defense. In contrast, while perception of fungal chitin does not promote sugar influx or SA accumulation, chitin-induced synthesis of the antifungal compound camalexin requires basal sugar influx activity. By monitoring sugar levels, plants determine defense levels and execute appropriate outputs against bacterial and fungal pathogens. Together, our findings provide a comprehensive view of the roles of sugar in defense."
Authors: Jordan Powers, Xing Zhang, Andres V. Reyes, Raul Zavaliev, Shou-Ling Xu and Xinnian Dong.
bioRxiv (2024)
Abstract: "For over 60 years, salicylic acid (SA) has been known as a plant immune signal required for both basal and systemic acquired resistance (SAR). SA activates these immune responses by reprogramming up to 20% of the transcriptome through the function of NPR1. However, components in the NPR1-signaling hub, which appears as nuclear condensates, and the NPR1-signaling cascade remained elusive due to difficulties in studying transcriptional cofactors whose chromatin associations are often indirect and transient. To overcome this challenge, we applied TurboID to divulge the NPR1-proxiome, which detected almost all known NPR1-interactors as well as new components of transcription-related complexes. Testing of new components showed that chromatin remodeling and histone demethylation contribute to SA-induced resistance. Globally, NPR1-proxiome shares a striking similarity to GBPL3-proxiome involved in SA synthesis, except associated transcription factors (TFs), suggesting that common regulatory modules are recruited to reprogram specific transcriptomes by transcriptional cofactors, like NPR1, through binding to unique TFs. Stepwise greenCUT&RUN analyses showed that, upon SA-induction, NPR1 initiates the transcriptional cascade primarily through association with TGA TFs to induce expression of secondary TFs, predominantly WRKYs. WRKY54 and WRKY70 then play a major role in inducing immune-output genes without interacting with NPR1 at the chromatin. Moreover, a loss of NPR1 condensate formation decreases its chromatin-association and transcriptional activity, indicating the importance of condensates in organizing the NPR1-signaling hub and initiating the transcriptional cascade. This study demonstrates how combinatorial applications of TurboID, and stepwise greenCUT&RUN transcend traditional genetic methods to globally map signaling hubs and transcriptional cascades."
Authors: Raul Zavaliev and Xinnian Dong.
Molecular Cell (2024)
Abstract: "Nonexpressor of pathogenesis-related genes 1 (NPR1) was discovered in Arabidopsis as an activator of salicylic acid (SA)-mediated immune responses nearly 30 years ago. How NPR1 confers resistance against a variety of pathogens and stresses has been extensively studied; however, only in recent years have the underlying molecular mechanisms been uncovered, particularly NPR1’s role in SA-mediated transcriptional reprogramming, stress protein homeostasis, and cell survival. Structural analyses ultimately defined NPR1 and its paralogs as SA receptors. The SA-bound NPR1 dimer induces transcription by bridging two TGA transcription factor dimers, forming an enhanceosome. Moreover, NPR1 orchestrates its multiple functions through the formation of distinct nuclear and cytoplasmic biomolecular condensates. Furthermore, NPR1 plays a central role in plant health by regulating the crosstalk between SA and other defense and growth hormones. In this review, we focus on these recent advances and discuss how NPR1 can be utilized to engineer resistance against biotic and abiotic stresses."
Authors: Qian Gong, Yunjing Wang, Xiaomeng Zhang, Jianjun Zhao, Yule Liu and Yiguo Hong.
Trends in Plant Science (2024)
Abstract: "Plants emit volatiles as signals to trigger broad physiological responses, including airborne defense (AD). Gong et al. (Nature 2023; 622: 139–145) recently reported the genetic framework of how plants use AD to combat aphids and viruses. The study elucidates the mutualistic relationships between aphids and the viruses they transmit, revealing the broad biological and ecological significance of AD."
Authors: Qian Gong, Yunjing Wang, Linfang He, Fan Huang, Danfeng Zhang, Yan Wang, Xiang Wei, Meng Han, Haiteng Deng, Lan Luo, Feng Cui, Yiguo Hong and Yule Liu.
Nature (2023)
Editor's view: Aphid-transmitted viruses encode proteins that suppress the plant airborne defence response—which is triggered by volatile chemicals released by neighbouring plants after aphid attack—and the plants consequently become less repellent to aphids and more suitable for aphid survival, infestation and viral transmission.
Abstract: "Aphids transmit viruses and are destructive crop pests1. Plants that have been attacked by aphids release volatile compounds to elicit airborne defence (AD) in neighbouring plants2–5. However, the mechanism underlying AD is unclear. Here we reveal that methyl-salicylate (MeSA), salicylic acid-binding protein-2 (SABP2), the transcription factor NAC2 and salicylic acid-carboxylmethyltransferase-1 (SAMT1) form a signalling circuit to mediate AD against aphids and viruses. Airborne MeSA is perceived and converted into salicylic acid by SABP2 in neighbouring plants. Salicylic acid then causes a signal transduction cascade to activate the NAC2–SAMT1 module for MeSA biosynthesis to induce plant anti-aphid immunity and reduce virus transmission. To counteract this, some aphid-transmitted viruses encode helicase-containing proteins to suppress AD by interacting with NAC2 to subcellularly relocalize and destabilize NAC2. As a consequence, plants become less repellent to aphids, and more suitable for aphid survival, infestation and viral transmission. Our findings uncover the mechanistic basis of AD and an aphid–virus co-evolutionary mutualism, demonstrating AD as a potential bioinspired strategy to control aphids and viruses."
Authors: Shan Liu, Faisal Islam, Jianping Chen, Zongtao Sun and Jian Chen.
Plant Communications (2024)
Excerpts: "Plants have evolved to generate and release a wide array of volatile organic compounds (VOCs) when challenged by environmental stimuli such as biotic and abiotic stresses, which facilitate their reproduction, defense responses, and plant-plant communication (Karban, 2021). Once emitted, some VOCs can elicit defense signaling in neighboring plants by interacting with specific receptor(s), a phenomenon referred to as airborne defense (AD) (Loreto and D’Auria, 2022)."
"MeSA plays important roles in plant AD. However, the mode of action of MeSA bridging interplant communication and inducing plant AD remains unclear. The recent study of Gong et al. (2023) unveiled an integral MeSA-mediated AD signal circuit composed of MeSA, salicylic acid-binding protein-2 (SABP2), the transcription factor NAC2, and salicylic acid-carboxylmethyltransferase-1 (SAMT1). This investigation deciphers the details of the molecular genetic mechanism by which MeSA is generated and perceived by neighboring plants as a plant AD agent (Gong et al., 2023)."
"In the interplay of aphid-plant-virus, aphid attack induces a high level of SA in plants, which activates NAC2-modulated SAMT1 transcription, thus upregulating biosynthesis and volatilization of MeSA, and conferring plant SAR against viruses (Figure 1A). As an airborne signal, volatile MeSA disperses and is then perceived by neighboring plants through the odorant-binding protein-like receptor SABP2, which converts MeSA into SA, leading to NAC2–SAMT1 activation to produce more MeSA against aphid infestation (Figure 1A). To counteract plant AD, CMV deploys a helicase domain-containing protein, possibly a conserved tactic among multiple virus species, to relocate and degrade NAC2 and thus promote aphid survival and virus infection by undermining the MeSA–SABP2–NAC2–SAMT1 signaling cascade (Figure 1B).
Authors: Nathan D. Meier, Kody Seward, Jeffrey L. Caplan and Savithramma P. Dinesh-Kumar.
Science Advances (2023)
Abstract: "Chloroplast morphology changes during immunity, giving rise to tubule-like structures known as stromules. Stromules extend along microtubules and anchor to actin filaments along nuclei to promote perinuclear chloroplast clustering. This facilitates the transport of defense molecules/proteins from chloroplasts to the nucleus. Evidence for a direct role for stromules in immunity is lacking since, currently, there are no known genes that regulate stromule biogenesis. We show that a calponin homology (CH) domain containing kinesin, KIS1 (kinesin required for inducing stromules 1), is required for stromule formation during TNL [TIR (Toll/Interleukin-1 receptor)-type nucleotide-binding leucine-rich repeat]-immune receptor-mediated immunity. Furthermore, KIS1 is required for TNL-mediated immunity to bacterial and viral pathogens. The microtubule-binding motor domain of KIS1 is required for stromule formation while the actin-binding, CH domain is required for perinuclear chloroplast clustering. We show that KIS1 functions through early immune signaling components, EDS1 and PAD4, with salicylic acid–induced stromules requiring KIS1. Thus, KIS1 represents a player in stromule biogenesis."
Authors: Isabel Monte.
Current Opinion in Plant Biology (2023)
Abstract: "The emergence of plant hormone signaling pathways is deeply intertwined with land plant evolution. In angiosperms, two plant hormones, salicylic Acid (SA) and Jasmonates (JAs), play a key role in plant defense, where JAs-mediated defenses are typically activated in response to herbivores and necrotrophic pathogens, whereas SA is prioritized against hemi/biotrophic pathogens. Thus, studying the evolution of SA and JAs and their crosstalk is essential to understand the evolution of molecular plant–microbe interactions (EvoMPMI) in land plants. Recent advances in the evolution of SA and JAs biosynthesis, signaling, and crosstalk in land plants illustrated that the insight gained in angiosperms does not necessarily apply to non-seed plant lineages, where the receptors perceive different ligands and the hormones activate pathways independently on the canonical receptors. In this review, recent findings on the two main defense hormones (JAs and SA) in non-seed plants, including functional studies in the bryophyte model Marchantia polymorpha, will be discussed."
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